Structural and functional insights into endoglin ligand recognition and binding

PLoS ONE

Volumn 7, Issue 2, 2012, Pages

  Alt, Aaron ^a   Miguel Romero, Laura ^a   Donderis, Jordi ^a,c   Aristorena, Mikel ^b,c   Blanco, Francisco J ^b,c   Round, Adam ^d   Rubio, Vicente ^a,c   Bernabeu, Carmelo ^b,c   Marina, Alberto ^a,c  

^a INSTITUTO DE BIOMEDICINA DE VALENCIA   (Spain)

^b CENTRO DE INVESTIGACIONES BIOLÓGICAS   (Spain)

^c INSTITUTO DE SALUD CARLOS III   (Spain)

^d EUROPEAN MOLECULAR BIOLOGY LABORATORY   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVIN RECEPTOR LIKE KINASE 1; BONE MORPHOGENETIC PROTEIN 9; ENDOGLIN; MONOMER; TRANSFORMING GROWTH FACTOR BETA; BMP10 PROTEIN, HUMAN; BMP8B PROTEIN, HUMAN; BONE MORPHOGENETIC PROTEIN; CELL SURFACE RECEPTOR; ENG PROTEIN, HUMAN; LEUKOCYTE ANTIGEN; LIGAND;

ARTICLE; CELL ASSAY; CELL STRAIN HEK293; COMPETITIVE INHIBITION; CONTROLLED STUDY; DIMERIZATION; DISULFIDE BOND; ECTODOMAIN; HUMAN; HUMAN CELL; LIGAND BINDING; MOLECULAR RECOGNITION; ORPHAN DOMAIN; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN GLYCOSYLATION; SURFACE PLASMON RESONANCE; X RAY CRYSTALLOGRAPHY; CHEMISTRY; METABOLISM; PROTEIN BINDING; PROTEIN MULTIMERIZATION;

ANTIGENS, CD; BONE MORPHOGENETIC PROTEINS; GROWTH DIFFERENTIATION FACTOR 2; HUMANS; LIGANDS; PROTEIN BINDING; PROTEIN MULTIMERIZATION; RECEPTORS, CELL SURFACE;

EID: 84856710142     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0029948     Document Type: Article

References (50)

1. Bernabeu C, Lopez-Novoa JM, Quintanilla M, (2009) The emerging role of TGF-beta superfamily coreceptors in cancer. Biochim Biophys Acta 1792: 954-973.
2. Lebrin F, Mummery CL, (2008) Endoglin-mediated vascular remodeling: mechanisms underlying hereditary hemorrhagic telangiectasia. Trends Cardiovasc Med 18: 25-32.
3. Lopez-Novoa JM, Bernabeu C, (2010) The physiological role of endoglin in the cardiovascular system. Am J Physiol Heart Circ Physiol 299: H959-974.
4. McAllister KA, Grogg KM, Johnson DW, Gallione CJ, Baldwin MA, et al. (1994) Endoglin, a TGF-beta binding protein of endothelial cells, is the gene for hereditary haemorrhagic telangiectasia type 1. Nat Genet 8: 345-351.
5. Bernabeu C, Blanco FJ, Langa C, Garrido-Martin EM, Botella LM, (2010) Involvement of the TGF-beta superfamily signalling pathway in hereditary haemorrhagic telangiectasia. J Appl Biomed 8: 169-171.
6. Shovlin CL, (2010) Hereditary haemorrhagic telangiectasia: pathophysiology, diagnosis and treatment. Blood Rev 24: 203-219.
7. Li C, Guo B, Bernabeu C, Kumar S, (2001) Angiogenesis in breast cancer: the role of transforming growth factor beta and CD105. Microsc Res Tech 52: 437-449.
8. Arthur HM, Ure J, Smith AJ, Renforth G, Wilson DI, et al. (2000) Endoglin, an ancillary TGFbeta receptor, is required for extraembryonic angiogenesis and plays a key role in heart development. Dev Biol 217: 42-53.
9. Bourdeau A, Dumont DJ, Letarte M, (1999) A murine model of hereditary hemorrhagic telangiectasia. J Clin Invest 104: 1343-1351.
10. Li DY, Sorensen LK, Brooke BS, Urness LD, Davis EC, et al. (1999) Defective angiogenesis in mice lacking endoglin. Science 284: 1534-1537.
11. Guerrero-Esteo M, Lastres P, Letamendia A, Perez-Alvarez MJ, Langa C, et al. (1999) Endoglin overexpression modulates cellular morphology, migration, and adhesion of mouse fibroblasts. Eur J Cell Biol 78: 614-623.
12. David L, Feige JJ, Bailly S, (2009) Emerging role of bone morphogenetic proteins in angiogenesis. Cytokine Growth Factor Rev 20: 203-212.
13. Lastres P, Letamendia A, Zhang H, Rius C, Almendro N, et al. (1996) Endoglin modulates cellular responses to TGF-beta 1. J Cell Biol 133: 1109-1121.
14. Blanco FJ, Santibanez JF, Guerrero-Esteo M, Langa C, Vary CP, et al. (2005) Interaction and functional interplay between endoglin and ALK-1, two components of the endothelial transforming growth factor-beta receptor complex. J Cell Physiol 204: 574-584.
15. Guerrero-Esteo M, Sanchez-Elsner T, Letamendia A, Bernabeu C, (2002) Extracellular and cytoplasmic domains of endoglin interact with the transforming growth factor-beta receptors I and II. J Biol Chem 277: 29197-29209.
16. Pardali E, Goumans MJ, ten Dijke P, (2010) Signaling by members of the TGF-beta family in vascular morphogenesis and disease. Trends Cell Biol 20: 556-567.
17. Finnson KW, Parker WL, ten Dijke P, Thorikay M, Philip A, (2008) ALK1 opposes ALK5/Smad3 signaling and expression of extracellular matrix components in human chondrocytes. J Bone Miner Res 23: 896-906.
18. David L, Mallet C, Mazerbourg S, Feige JJ, Bailly S, (2007) Identification of BMP9 and BMP10 as functional activators of the orphan activin receptor-like kinase 1 (ALK1) in endothelial cells. Blood 109: 1953-1961.
19. Scharpfenecker M, van Dinther M, Liu Z, van Bezooijen RL, Zhao Q, et al. (2007) BMP-9 signals via ALK1 and inhibits bFGF-induced endothelial cell proliferation and VEGF-stimulated angiogenesis. J Cell Sci 120: 964-972.
20. Suzuki Y, Ohga N, Morishita Y, Hida K, Miyazono K, et al. (2010) BMP-9 induces proliferation of multiple types of endothelial cells in vitro and in vivo. J Cell Sci 123: 1684-1692.
21. Upton PD, Davies RJ, Trembath RC, Morrell NW, (2009) Bone morphogenetic protein (BMP) and activin type II receptors balance BMP9 signals mediated by activin receptor-like kinase-1 in human pulmonary artery endothelial cells. J Biol Chem 284: 15794-15804.
22. Ricard N, Bidart M, Mallet C, Lesca G, Giraud S, et al. (2010) Functional analysis of the BMP9 response of ALK1 mutants from HHT2 patients: a diagnostic tool for novel ACVRL1 mutations. Blood 116: 1604-1612.
23. Gougos A, Letarte M, (1990) Primary structure of endoglin, an RGD-containing glycoprotein of human endothelial cells. J Biol Chem 265: 8361-8364.
24. Jovine L, Qi H, Williams Z, Litscher E, Wassarman PM, (2002) The ZP domain is a conserved module for polymerization of extracellular proteins. Nat Cell Biol 4: 457-461.
25. Llorca O, Trujillo A, Blanco FJ, Bernabeu C, (2007) Structural model of human endoglin, a transmembrane receptor responsible for hereditary hemorrhagic telangiectasia. J Mol Biol 365: 694-705.
26. Plaza S, Chanut-Delalande H, Fernandes I, Wassarman PM, Payre F, (2010) From A to Z: apical structures and zona pellucida-domain proteins. Trends Cell Biol 20: 524-532.
27. Van Le B, Franke D, Svergun DI, Han T, Hwang HY, et al. (2009) Structural and functional characterization of soluble endoglin receptor. Biochem Biophys Res Commun 383: 386-391.
28. Castonguay R, Werner ED, Matthews RG, Presman E, Mulivor AW, et al. (2011) Soluble endoglin specifically binds BMP9/BMP10 via its orphan domain,inhibits blood vessel formation and suppresses tumor growth. J Biol Chem 286: 30034-30046.
29. Basile G, Peticca M, Cusano P, Catello S, (2009) Yeast-secreted recombinant extracellular domain of human CD105 antigen is able to bind TGF-beta type II receptor in vitro. Mol Biotechnol 41: 26-34.
30. Pichuantes S, Vera S, Bourdeau A, Pece N, Kumar S, et al. (1997) Mapping epitopes to distinct regions of the extracellular domain of endoglin using bacterially expressed recombinant fragments. Tissue Antigens 50: 265-276.
31. Takacs E, Barabas O, Petoukhov MV, Svergun DI, Vertessy BG, (2009) Molecular shape and prominent role of beta-strand swapping in organization of dUTPase oligomers. FEBS Lett 583: 865-871.
32. Berrow NS, Alderton D, Owens RJ, (2009) The precise engineering of expression vectors using high-throughput In-Fusion PCR cloning. Methods Mol Biol 498: 75-90.
33. Reeves PJ, Callewaert N, Contreras R, Khorana HG, (2002) Structure and function in rhodopsin: high-level expression of rhodopsin with restricted and homogeneous N-glycosylation by a tetracycline-inducible N-acetylglucosaminyltransferase I-negative HEK293S stable mammalian cell line. Proc Natl Acad Sci U S A 99: 13419-13424.
34. Chang VT, Crispin M, Aricescu AR, Harvey DJ, Nettleship JE, et al. (2007) Glycoprotein structural genomics: solving the glycosylation problem. Structure 15: 267-273.
35. Raab U, Velasco B, Lastres P, Letamendia A, Cales C, et al. (1999) Expression of normal and truncated forms of human endoglin. Biochem J 339 (Pt 3): 579-588.
36. Mitchell D, Pobre EG, Mulivor AW, Grinberg AV, Castonguay R, et al. (2010) ALK1-Fc inhibits multiple mediators of angiogenesis and suppresses tumor growth. Mol Cancer Ther 9: 379-388.
37. Barbara NP, Wrana JL, Letarte M, (1999) Endoglin is an accessory protein that interacts with the signaling receptor complex of multiple members of the transforming growth factor-beta superfamily. J Biol Chem 274: 584-594.
38. Letamendia A, Lastres P, Botella LM, Raab U, Langa C, et al. (1998) Role of endoglin in cellular responses to transforming growth factor-beta. A comparative study with betaglycan. J Biol Chem 273: 33011-33019.
39. Lin SJ, Hu Y, Zhu J, Woodruff TK, Jardetzky TS, (2011) Structure of betaglycan zona pellucida (ZP)-C domain provides insights into ZP-mediated protein polymerization and TGF-beta binding. Proc Natl Acad Sci U S A 108: 5232-5236.
40. Korchynskyi O, ten Dijke P, (2002) Identification and functional characterization of distinct critically important bone morphogenetic protein-specific response elements in the Id1 promoter. J Biol Chem 277: 4883-4891.
41. Mertens HD, Svergun DI, (2010) Structural characterization of proteins and complexes using small-angle X-ray solution scattering. J Struct Biol 172: 128-141.
42. Roy A, Kucukural A, Zhang Y, (2010) I-TASSER: a unified platform for automated protein structure and function prediction. Nat Protoc 5: 725-738.
43. Kim DE, Chivian D, Baker D, (2004) Protein structure prediction and analysis using the Robetta server. Nucleic Acids Res 32: W526-531.
44. Lutteke T, Bohne-Lang A, Loss A, Goetz T, Frank M, et al. (2006) GLYCOSCIENCES.de: an Internet portal to support glycomics and glycobiology research. Glycobiology 16: 71R-81R.
45. Hammond C, Braakman I, Helenius A, (1994) Role of N-linked oligosaccharide recognition, glucose trimming, and calnexin in glycoprotein folding and quality control. Proc Natl Acad Sci U S A 91: 913-917.
46. Mitra N, Sinha S, Ramya TN, Surolia A, (2006) N-linked oligosaccharides as outfitters for glycoprotein folding, form and function. Trends Biochem Sci 31: 156-163.
47. Cannon JP, O'Driscoll M, Litman GW, (2011) Construction, expression, and purification of chimeric protein reagents based on immunoglobulin fc regions. Methods Mol Biol 748: 51-67.
48. Schrödinger LLC, (2006) The PyMOL Molecular Graphics System. Schrödinger LLC.
49. Pernot P, Round A, Theveneau P, Giraud T, Nogueira-Fernandes R, et al. (2010) New beamline dedicated to solution scattering from biological macromolecules at the ESRF. J Phys: Conf Ser 247: 012009.
50. Kelley LA, Sternberg MJ, (2009) Protein structure prediction on the Web: a case study using the Phyre server. Nat Protoc 4: 363-371.